Metabolic reprogramming of tomato plants under Ralstonia solanacearum infection

• Tomato cultivar Hawaii 7998 showed superior resistance with distinct metabolic profiles compared to susceptible Kashi Adarsh • Metabolomics identified metabolites showing temporal and cultivar-specific regulation patterns • Key defense pathways including phenylpropanoid, flavonoid and fatty acid metabolism were upregulated during infection • Enhanced antioxidant activities in Hawaii 7998 correlated with improved disease resistance • Solasodine, biotin, riboflavin, tryptophan, naringin, uridine, phosphatidylcholine and linolenic acid represented cultivar-specific metabolite biomarkers • Pathogen-interaction specific biomarkers included solasodine, biotin, asparagine, coumaryl alcohol, zeaxanthin and inosine • Network analysis showed regulatory nodes in carotenoid, trehalose and phenylpropanoid pathways during infection Comprehensive metabolomic investigation of tomato ( Solanum lycopersicum ) cultivar Hawaii 7998 and variety Kashi Adarsh was performed to establish metabolic basis of resistance and susceptibility against bacterial wilt pathogen Ralstonia solanacearum . Using LC-MS/MS-based untargeted metabolomics, leaf samples were analyzed at 5 and 10-day post-inoculation, revealing significant metabolic distinctions between the plants. The resistant cultivar Hawaii 7998 demonstrated remarkably lower disease incidence (15.19%) compared to the susceptible variety (86.81%) underpinned by distinct metabolic profiles. Our analysis annotated metabolites across different treatment groups, with significant differential regulation in pathways related to phenylpropanoids, flavonoids, and primary metabolism. Hawaii 7998 exhibited higher constitutive levels of defense-related compounds and mounted more robust metabolic responses against the pathogen. The resistant cultivar Hawaii 7998 under non-treated condition showed enhanced accumulation of total phenolic content (32.81 and 35.17 mg GAE g -1 at 5 and 10DAI respectively) compared to susceptible plants. High antioxidant activities in terms of DPPH (43.52 and 47.19% in non-inoculated and 56.74 and 66.75% in pathogen inoculated condition at 5 and 10DAI respectively) and ABTS (44.36 and 48.06% in control and 58.24 and 64.05% in treated plants) were observed in Hawaii 7998, which was significantly high as compared to Kashi Adarsh. Network analysis showed complex interactions between metabolic pathways, highlighting key regulatory nodes in disease resistance, including carotenoid biosynthesis, trehalose metabolism, and phenylpropanoid pathways. Annotation of biomarker metabolites that included solasodine, biotin, uridine, phosphatidylcholine, asparagine, coumaryl alcohol and linolenic acid revealed cultivar-specific and pathogen interaction specific biomarkers in tomato. These findings are particularly significant in the uncovering the molecular mechanisms of plant-pathogen interaction and offer crucial insights for developing bacterial wilt-resistant tomato varieties, thereby contributing to food security.